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PMID: 11782547 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Translocation of Cockayne syndrome group A protein to the nuclear matrix: possible relevance to transcription-coupled DNA repair.

Kamiuchi S, Saijo M, Citterio E, de Jager M, Hoeijmakers JH, Tanaka K

Abstract

Transcription-coupled repair (TCR) efficiently removes a variety of lesions from the transcribed strand of active genes. By allowing rapid resumption of RNA synthesis, the process is of major importance for cellular resistance to transcription-blocking genotoxic damage. Mutations in the Cockayne syndrome group A or B (CSA or CSB) gene result in defective TCR. However, the exact mechanism of TCR in mammalian cells remains to be elucidated. We found that CSA protein is rapidly translocated to the nuclear matrix after UV irradiation. The translocation of CSA was independent of Xeroderma pigmentosum group C, which is specific to the global genome repair subpathway of nucleotide excision repair (NER) and of the core NER factor Xeroderma pigmentosum group A but required the CSB protein. In UV-irradiated cells, CSA protein colocalized with the hyperphosphorylated form of RNA polymerase II, engaged in transcription elongation. The translocation of CSA was also induced by treatment of the cells with cisplatin or hydrogen peroxide, both of which produce damage that is subjected to TCR but not induced by treatment with dimethyl sulfate, which produces damage that is not subjected to TCR. The hydrogen peroxide-induced translocation of CSA was also CSB dependent. These findings establish a link between TCR and the nuclear matrix mediated by CSA.

MeSH Terms
Active Transport, Cell Nucleus Alkylating Agents/pharmacology Cell Line Cell Nucleus/metabolism Cisplatin/pharmacology DNA Repair DNA Repair Enzymes HeLa Cells Humans Hydrogen Peroxide/pharmacology Microscopy, Fluorescence Mutagens/pharmacology Oxidants/pharmacology Phosphorylation Protein Transport Proteins/genetics,metabolism Radiation-Sensitizing Agents/pharmacology Subcellular Fractions/metabolism Sulfuric Acid Esters/pharmacology Time Factors Transcription Factors Transcription, Genetic Transfection Ultraviolet Rays
Chemicals
Alkylating Agents ERCC8 protein, human Mutagens Oxidants Proteins Radiation-Sensitizing Agents Sulfuric Acid Esters Transcription Factors Hydrogen Peroxide DNA Repair Enzymes dimethyl sulfate Cisplatin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kamiuchi Shinya
Division of Cellular Genetics, Institute for Molecular and Cellular Biology, Osaka University and Core Research for Evolutional Science and Technology (CREST), Japan.
Saijo Masafumi
Citterio Elisabetta
de Jager Martijn
Hoeijmakers Jan H J
Tanaka Kiyoji
References (42)
42 references, click to expand
  1. A nuclear matrix protein interacts with the phosphorylated C-terminal domain of RNA polymerase II.
    Mol Cell Biol. 1998 Apr;18(4):2406-15 PMID: 9528809
  2. BRCA1 required for transcription-coupled repair of oxidative DNA damage.
    Science. 1998 Aug 14;281(5379):1009-12 PMID: 9703501
  3. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair.
    Mol Cell. 1998 Aug;2(2):223-32 PMID: 9734359
  4. RNA polymerase II elongation complexes containing the Cockayne syndrome group B protein interact with a molecular complex containing the transcription factor IIH components xeroderma pigmentosum B and p62.
    J Biol Chem. 1998 Oct 23;273(43):27794-9 PMID: 9774388
  5. Molecular mechanism of nucleotide excision repair.
    Genes Dev. 1999 Apr 1;13(7):768-85 PMID: 10197977
  6. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta.
    Nature. 1999 Jun 17;399(6737):700-4 PMID: 10385124
  7. Three-dimensional visualization of transcription sites and their association with splicing factor-rich nuclear speckles.
    J Cell Biol. 1999 Aug 9;146(3):543-58 PMID: 10444064
  8. Replication of damaged DNA: molecular defect in xeroderma pigmentosum variant cells.
    Mutat Res. 1999 Oct 22;435(2):111-9 PMID: 10556591
  9. Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK.
    Genes Dev. 2000 Feb 1;14(3):349-59 PMID: 10673506
  10. The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA.
    J Biol Chem. 2000 Mar 31;275(13):9870-5 PMID: 10734143
  11. Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome.
    Cell. 2000 Apr 14;101(2):159-71 PMID: 10786832
  12. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor.
    Mol Cell Biol. 2000 Oct;20(20):7643-53 PMID: 11003660
  13. XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription.
    J Biol Chem. 2000 Nov 10;275(45):34931-7 PMID: 10944529
  14. In vitro transcription: whole-cell extract.
    Methods Enzymol. 1983;101:568-82 PMID: 6193397
  15. Lesions induced in DNA by ultraviolet light are repaired at the nuclear cage.
    J Cell Sci. 1984 Aug;70:189-96 PMID: 6501435
  16. Intranuclear localization of UV-induced DNA repair in human VA13 cells.
    Mutat Res. 1987 Mar;183(2):177-84 PMID: 3029583
  17. The localization of ultraviolet-induced excision repair in the nucleus and the distribution of repair events in higher order chromatin loops in mammalian cells.
    J Cell Sci Suppl. 1987;6:243-62 PMID: 3477564
  18. Nuclear matrix associated DNA is preferentially repaired in normal human fibroblasts, exposed to a low dose of ultraviolet light but not in Cockayne's syndrome fibroblasts.
    Nucleic Acids Res. 1988 Nov 25;16(22):10607-22 PMID: 3205718
  19. Repair of N-methylpurines in specific DNA sequences in Chinese hamster ovary cells: absence of strand specificity in the dihydrofolate reductase gene.
    Proc Natl Acad Sci U S A. 1989 May;86(9):3050-4 PMID: 2785688
  20. Core filaments of the nuclear matrix.
    J Cell Biol. 1990 Mar;110(3):569-80 PMID: 2307700
  21. The genetic defect in Cockayne syndrome is associated with a defect in repair of UV-induced DNA damage in transcriptionally active DNA.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4707-11 PMID: 2352945
  22. Repair of individual DNA strands in the hamster dihydrofolate reductase gene after treatment with ultraviolet light, alkylating agents, and cisplatin.
    J Biol Chem. 1993 Jan 25;268(3):1650-7 PMID: 8420940
  23. Molecular mechanism of transcription-repair coupling.
    Science. 1993 Apr 2;260(5104):53-8 PMID: 8465200
  24. Cockayne syndrome: review of 140 cases.
    Am J Med Genet. 1992 Jan 1;42(1):68-84 PMID: 1308368
  25. Preferential repair of ionizing radiation-induced damage in the transcribed strand of an active human gene is defective in Cockayne syndrome.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10499-503 PMID: 8248136
  26. Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells.
    Nucleic Acids Res. 1993 Dec 25;21(25):5890-5 PMID: 8290349
  27. Reconstitution of human DNA repair excision nuclease in a highly defined system.
    J Biol Chem. 1995 Feb 10;270(6):2415-8 PMID: 7852297
  28. Mammalian DNA nucleotide excision repair reconstituted with purified protein components.
    Cell. 1995 Mar 24;80(6):859-68 PMID: 7697716
  29. The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH.
    Cell. 1995 Aug 25;82(4):555-64 PMID: 7664335
  30. Transcription-coupled repair deficiency and mutations in human mismatch repair genes.
    Science. 1996 Apr 26;272(5261):557-60 PMID: 8614807
  31. A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8253-7 PMID: 8710856
  32. Ultraviolet-induced movement of the human DNA repair protein, Xeroderma pigmentosum type G, in the nucleus.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8368-73 PMID: 8710877
  33. Recruitment of damaged DNA to the nuclear matrix in hamster cells following ultraviolet irradiation.
    Nucleic Acids Res. 1996 Aug 1;24(15):2877-84 PMID: 8760868
  34. Mutational analysis of the human nucleotide excision repair gene ERCC1.
    Nucleic Acids Res. 1996 Sep 1;24(17):3370-80 PMID: 8811092
  35. Human transcription-repair coupling factor CSB/ERCC6 is a DNA-stimulated ATPase but is not a helicase and does not disrupt the ternary transcription complex of stalled RNA polymerase II.
    J Biol Chem. 1997 Jan 17;272(3):1885-90 PMID: 8999876
  36. Components of the human SWI/SNF complex are enriched in active chromatin and are associated with the nuclear matrix.
    J Cell Biol. 1997 Apr 21;137(2):263-74 PMID: 9128241
  37. Translocation of a UV-damaged DNA binding protein into a tight association with chromatin after treatment of mammalian cells with UV light.
    J Cell Sci. 1997 May;110 ( Pt 10):1159-68 PMID: 9191040
  38. Differential involvement of the human mismatch repair proteins, hMLH1 and hMSH2, in transcription-coupled repair.
    Cancer Res. 1997 Sep 1;57(17):3784-91 PMID: 9288788
  39. The Cockayne syndrome B protein, involved in transcription-coupled DNA repair, resides in an RNA polymerase II-containing complex.
    EMBO J. 1997 Oct 1;16(19):5955-65 PMID: 9312053
  40. Cockayne syndrome group B protein enhances elongation by RNA polymerase II.
    Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11205-9 PMID: 9326587
  41. Recruitment of the putative transcription-repair coupling factor CSB/ERCC6 to RNA polymerase II elongation complexes.
    Mol Cell Biol. 1997 Dec;17(12):6803-14 PMID: 9372911
  42. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors.
    EMBO J. 1997 Nov 3;16(21):6559-73 PMID: 9351836
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-01-08
Pages
201-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC117539
Subset
IM
Grants
NIA NIH HHS · P01 AG017242 · United States
NIA NIH HHS · AG17242-02 · United States
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